Water Permeability of Palaemon Longirostris and Other Euryhaline Caridean Prawns
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J. exp. Biol. ISO, 145-158 (1990) 145 {Printed in Great Britain © The Company of Biologists Limited 1990 WATER PERMEABILITY OF PALAEMON LONGIROSTRIS AND OTHER EURYHALINE CARIDEAN PRAWNS BY PETER J. CAMPBELL AND M. B. JONES Department of Biological Sciences, Polytechnic South West, Drake Circus, Plymouth PL4 8AA, England Accepted 6 February 1990 Summary Water permeability [based on the half-time of exchange of body water with the environment (7\/2)] of the upper estuarine prawn Palaemon longirostris was measured in a range of salinities at 4, 12 and 20°C. Prawns acclimated for 7 days were compared with prawns exposed to acute salinity changes. Acclimation to low salinity and low temperature caused a significant reduction in permeability. Transfer of prawns from 34 to 0.5 %o had no immediate effect on permeability; however, transfer from 0.5 to 34 %o caused an immediate significant rise in permeability. Heart rate of P. longirostris acclimated to 0.5 and 34 %o at 4, 12 and 20°C was unaffected by salinity, but was significantly reduced at low temperature. The permeabilities of three other prawn species (Palaemonetes varians, Cran- gon crangon and Palaemon elegans), which have different horizontal distributions in estuaries and different salinity tolerance ranges, were also studied and compared with the values obtained for P. longirostris. P. varians and C. crangon showed significantly reduced permeabilities at low compared with high salinities; however, the permeability of P. elegans was unchanged at the two salinities used for this species (22 and 34 %o). At each experimental salinity, permeabilities followed the sequence: P. longirostris<P. varians<C. crangon<P. elegans. Results show that reduction of permeability is an important physiological adaptation to life in dilute saline regions and may be involved in separating species with overlapping salinity tolerance ranges. Introduction Crustaceans living in hypo-osmotic environments lose salts and gain water, but have physiological mechanisms that compensate for these exchanges and maintain hyperosmotic body fluids (Gilles, 1975; Kirschner, 1979; Mantel and Farmer, 1983; Greenaway, 1979; Spaargaren, 1979). Rates of water gain and salt loss may be limited by lowering the permeability of the body surface (Lockwood, 1976), and there is a general trend amongst crustaceans of a less permeable body surface as the osmotic gradient between the body fluids and the external medium increases (Potts and Parry, 1964; Rudy, 1967; Bolt, 1983, 1989). Indeed, reduction of fctey words: water permeability, salinity, temperature, Palaemon longirostris, Palaemonetes Warians, Crangon crangon, Palaemon elegans, habitat. 146 P. J. CAMPBELL AND M. B. JONES surface permeability is considered to be a major adaptation to life away from the sea. Animals living under conditions of fluctuating salinity would also clearly benefit from an ability to alter surface permeability, and such flexibility would require a mechanism sensitive to the concentration between the blood and the external medium (Bolt, 1983). Examples of euryhaline crustaceans with this ability are limited but include the crabs Carcinus maenas (Smith, 1970), Rhithropanopeus harrisi (Smith, 1967) and Hemigrapsus nudus (Smith and Rudy, 1972) and the amphipods Gammarus duebeni (Lockwood and Inman, 1973; Bolt et al. 1980; Bolt, 1983) and Corophium volutator (Taylor, 1985). Palaemon longirostris (Milne Edwards) occupies the upper, dilute saline regions of large river estuaries (Smaldon, 1979). It has a salinity tolerance range between 0.5 and 43 %o (Campbell and Jones, 1990) and maintains almost constant haemolymph osmotic and ionic concentrations over this wide salinity range (Campbell and Jones, 1989a,b). The present study investigates the changes in water permeability of P. longirostris acclimated to different salinities and exposed to sudden salinity change. Since temperature affects the osmotic and ionic regulation of P. longirostris (Campbell and Jones, 1989a,b), the influence of temperature on the water permeability of P. longirostris is reported also. The permeabilities of three other prawn species [Palaemonetes varians (Leach), Crangon crangon (Linnaeus) and Palaemon elegans (Rathke)] were studied and compared with the observations on P. longirostris. All are euryhaline but they have different salinity tolerance ranges and habitats. P. varians occurs in brackish- water pools indirectly connected to the sea and tolerates salinities between 1 and 30 %o (Hagerman and Uglow, 1983). C. crangon occupies the lower reaches of estuaries and tolerates salinities between 5 and 39 %o (Broekema, 1941). P. elegans is essentially an intertidal species and has a salinity tolerance range between 5 and 45 %o (Ramirez de Isla Hernandez and Taylor, 1985). Materials and methods Animal husbandry All these prawn species occur within the River Tamar Estuary, Plymouth, but in different regions. Palaemon longirostris were collected from the upper reaches at Calstock, Crangon crangon from the lower reaches at Cargreen and Palaemonetes varians from brackish-water pools at St Johns Lake. Palaemon elegans occurs around the estuary mouth but, as access to suitable sites was limited, prawns were taken from intertidal rockpools at Wembury. They were hand-netted at low tide and transported back to the laboratory in habitat water. They were maintained in plastic aquaria supplied with continuously flowing sea water (salinity 34 %o; temperature 12°C) and fed once a week on mussel (Mytilus edulis L.) or fish (Gadus sp.). For each species, 10 intermoult prawns of carapace length 18-24 mm (measured from rostral tip to posterior carapace edge) were acclimated for 7 days to an experimental salinity at 4,12 or 20°C (to ±1°C) (temperature was controlled with the use of constant-temperature water baths). Prawns were held in plastS Permeability of euryhaline prawns \A1 aquaria (501) supplied with continuously aerated, recycled water at the appropri- ate salinity and temperature. They were subjected to a 12h light: 12h dark cycle, and were not fed for 3 days prior to or during the experiments. Steady-state salinity experiments Permeability was determined by measuring the time taken for half the body water to exchange with the external medium (7\/2), using tritiated water (THO) as a tracer (Lockwood et al. 1973). This method of determining water permeability has certain limitations since it does not take into account either boundary layer resistance (both inside and outside the animal) or bulk flow through pores (Lockwood et al. 1973). For these reasons, the term 'apparent water permeability' (AWP) is used when referring to permeability determined by the THO outflux technique (Smith, 1967). Tests by Bolt (1983), however, have shown that measurements of 7\/2 using THO were comparable to those based on direct urine measurements, suggesting that changes in water permeability using THO as a marker do reflect real changes in the water permeability of an animal. Water permeability of Palaemon longirostris was measured at 12°C in 0.5, 7.0, 22.0, 34.0 and 43.0 %o, and at 4 and 20°C in 0.5 and 34 %o. Water permeability was also determined at 12 °C for Palaemonetes varians in 0.5 and 34 %o, Crangon crangon in 7, 22 and 34 %o and Palaemon elegans in 22 and 34 %o. Prawns were transferred from the acclimation aquaria to screw-top glass jars containing 250 ml of THO (50 (id ml"1) of the same salinity and temperature as in the acclimation medium and left to load for a minimum period of 5 h. They were then removed and thoroughly rinsed with 600 ml of water of the appropriate salinity and temperature. Prawns were subsequently blotted dry with absorbent tissue and transferred to a blank unloading medium containing 250 ml of water at the same salinity and temperature as the loading medium. This unloading medium was contained within screw-top jars to prevent any exchange of THO with water vapour in the air. The time of immersion in the unloading medium was noted and 100/il samples were taken 2, 4, 8, 16, 32 and 64min after immersion (Ct). The samples were placed into 4 ml of a liquid scintillation cocktail (cocktail 'Ex' Scintran, BDH) and counted using a liquid scintillation counter (Philips, model PW4700). Tests by Lockwood et al. (1973) showed that quenching of the counts due to differences in the salinity of the external medium were negligible. The last sample was taken when the THO in the animal was in equilibrium with the external medium (C=c) and this is equivalent to more than 10x7\/2. log(Co<, — Ct) was plotted against time and, if the permeability was constant throughout the experiment, the result was a straight line. Using a regression line fitted to the data, the time taken for half the body water to be exchanged with the external medium (7\/2) was calculated by taking the x value of the y point corresponding to logCoo-log2. The correlation coefficient of the straight line was generally greater tfian 0.98, so only two C, values needed to be taken at a time close to that of the Ti/2 to fit a regression line to the data. This short cut, however, could only be 148 P. J. CAMPBELL AND M. B. JONES taken when the approximate 7\/2 was known (e.g. when experiments were replicated for prawns at the same salinity/temperature combination). Sudden salinity transfer Changes in permeability of Palaemon longirostris acclimated for 7 days to 34 and 0.5 %o, and transferred directly to 0.5 and 34 %o, respectively, were measured in 10 prawns at 12°C. Water permeability was determined by measuring the 7\/2 for THO ourflux using the same method as described in the previous section, except that prawns loaded in 34 %o were unloaded in 0.5 %o and vice versa. Heart rate in Palaemon longirostris The heart rates of five prawns acclimated to each combination of salinity (0.5 and 34 %o) and temperature (4, 12 and 20 °C) were measured using an impedance technique (Johnson, 1985).